epigenetic mechanisms: mediating between experience & mental & physical health

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M M M M M M Epigenetic mechanisms mediating between experience and mental and physical health Moshe Szyf Department of Pharmacology and Therapeutics McGill University, Montreal Canada The Science of Hope Foundation for healthy generations Seattle, Washington, April 19 2016

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Page 1: Epigenetic Mechanisms: Mediating Between Experience & Mental & Physical Health

M M M MMM

Epigenetic mechanisms mediating between experience and mental and physical health

Moshe Szyf

Department of Pharmacology and Therapeutics

McGill University, Montreal Canada

The Science of HopeFoundation for healthy generations Seattle, Washington,

April 19 2016

Page 2: Epigenetic Mechanisms: Mediating Between Experience & Mental & Physical Health

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DNA METHYLATION REACTIONS

Page 3: Epigenetic Mechanisms: Mediating Between Experience & Mental & Physical Health

Epigenetic marks (i.e. DNA methylation) at critical positions silence genes;

same gene could be either active or silent based on the state of methylation

X

Tet H2OH

X

Page 4: Epigenetic Mechanisms: Mediating Between Experience & Mental & Physical Health

DNA methylation inhibits RNA Pol2 complex binding

.TBP

TBP

Page 5: Epigenetic Mechanisms: Mediating Between Experience & Mental & Physical Health

CH3

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CH3

me

thy

las

e

de

me

thy

las

e

active

inactive

The gene is an equilibrium between activity and lack of activity that is defined by

epigenetic marks. Epigenetic marks program how genes work in different organs

in our body;

This equilibrium could be reset by environmental signals

nutrients

toxinssocial

behavioral pathological

physiological

Page 6: Epigenetic Mechanisms: Mediating Between Experience & Mental & Physical Health

DNA METHYLATION a mechanism of adaptation of the genome

in response to changing environments without changing the

sequence of DNA

•Evolutionary time scale

•Trans-generational time scale

•Life long time scale

•Life cycle stations time scale

•Seasonal time scale

•Physiological proximal time scale

Page 7: Epigenetic Mechanisms: Mediating Between Experience & Mental & Physical Health

Bioenvironment Physical environment Social environment

phenotype

Bioenvironment Physical environment Social environment

Health challenges

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System wide

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Signaling pathways

Adaptive response of the genome in early life

Page 8: Epigenetic Mechanisms: Mediating Between Experience & Mental & Physical Health

LOW LG HIGH LG

STRESS RESPONSE STRESS RESPONSE

A bar in Madrid, licking rats and the birth of the field of “behavioral epigenetics”

Pups

Adults

Page 9: Epigenetic Mechanisms: Mediating Between Experience & Mental & Physical Health

Biological mother Adoptive mother

Low LG

Low LGHigh LG

High LG

Behavioral programming by the mother is epigenetic not genetic;

The fostering mother and not the biological mothers transfers the phenotype

Cross-fostering /adoption

experiment

Page 10: Epigenetic Mechanisms: Mediating Between Experience & Mental & Physical Health

PKA

Behavioral gene programming is stable but nevertheless reversible

5-HT

cAMP

NGFI-A

HAT

DemethylaseMBD2?

DNMT

TSA

Methionine

Page 11: Epigenetic Mechanisms: Mediating Between Experience & Mental & Physical Health

The signature of maternal care in non-

human primates

Mother Surrogate

Stephen Suomi

Page 12: Epigenetic Mechanisms: Mediating Between Experience & Mental & Physical Health

Genome wide view of the differential methylation between maternal and nursery reared rhesus monkeys in T cells and

prefrontal cortex

Page 13: Epigenetic Mechanisms: Mediating Between Experience & Mental & Physical Health

PROMOTER METHYLATION RESPONSE TO early life stress Maternal deprivation in

T CELLS AND PFC

Rearing = mother

/ nursery

high

low

me

thylatio

nPFC T cells

Page 14: Epigenetic Mechanisms: Mediating Between Experience & Mental & Physical Health

Quebec ice storm 1998

Storm32 score

ThreatLoss

Scope Change

Page 15: Epigenetic Mechanisms: Mediating Between Experience & Mental & Physical Health

DNA methylation signatures of randomized objective stress during pregnancy in

human adolescent T cells Quebec ice storm of 1998

storm32

44

9

30

120

6

87

9

70

9

94

8

136

8

13

5

28

7

51

121

0

38

4

39 8

119

1

124

8

20

4

82

6 9

11

5

136

5

82

7

139

1

115

7

40

5

131

6

131

5

56

142

7

106

0

10

5

103

0

103

6

36

3

100 C

pG

sites

storm32 heatmap

storm32

1206

1206

709

449

30

879

1368

51

135

287

948

948

1210

384

39

1191 8

204

826 9

827

1316

1315

115

1365

405

1248

1391

1157

1427

56

1030

105

1060

1036

363

promoters

storm32 heatmap

stress%low%medium%high%

high%

low%

methyla1

on%

samples%

CpG%sites%

The$DNA$methylation$signature$of$maternal$stress$in$chord$blood$T$cells:

Page 16: Epigenetic Mechanisms: Mediating Between Experience & Mental & Physical Health

Correlation between objective randomized stress during pregnancy and CG methylation

in the SCG5 gene in T cells of 15 year old

Objective stress during ice storm 1998

Meth

yla

tio

n

Page 17: Epigenetic Mechanisms: Mediating Between Experience & Mental & Physical Health

Ice storm data suggested enrichment of type 1 diabetes pathway

Type 1 diabetes signaling pathway enriched with differentially methylated genes that correlate with objective stress

Page 18: Epigenetic Mechanisms: Mediating Between Experience & Mental & Physical Health

DNA methylation mediates the long term impact of

adult experience, for example, chronic pain, addiction;

Diagnostic and therapeutic implications

Page 19: Epigenetic Mechanisms: Mediating Between Experience & Mental & Physical Health

Transcription

factorX

CH3 CH3

X

Transcription

factor

XAcAc Ac

Transcription

Machinery

Transcription

machineryDNMT

Demethylases

Protein A Protein AX

Phenotype A Phenotype B

RG108

SAM

Behavioral intervention

Page 20: Epigenetic Mechanisms: Mediating Between Experience & Mental & Physical Health

Transcription

factorX

CH3 CH3

X

Transcription

factor

XAcAc Ac

Transcription

Machinery

Transcription

machineryDNMT

Demethylases

Protein A Protein AX

Phenotype A Phenotype B

Figure 1

RG108

SAM

Behavioral intervention

Page 21: Epigenetic Mechanisms: Mediating Between Experience & Mental & Physical Health

Incubation model of cocaine craving

Copyright 2013, Western Washington University,

Behavioral Neuroscience Program/Grimm lab

RG108, SAM or aCSF

injections

Days

cocaine (Coc.) or saline (Sal.)

self-administration (SA)

withdrawal

10 days0 1 Day 30

Day 1 groups:- Sal. SA: Sal.- Coc. SA no cue: 1W- Coc. SA cue: 1C

Day 30 groups:- Coc. SA no cue: 30W- Coc. SA cue: 30C+- Coc. SA cue-aCSF: aCSF- Coc. SA cue-RG108 cue: RG108- Coc. SA cue-SAM: SAM- Coc. SA cue-PPT- Coc. SA cue-roscovitine

RG108 or aCSFinjections

Days

10 days

0-2cocaine

self-administration

a

b

FIGURE 1

Day 60

withdrawal

Day 60 groups:

- Coc. SA cue-aCSF: aCSF-60

- Coc. SA cue-RG108 cue: RG108-60

- Coc. SA cue-SAM: SAM-60

EPM, locomotion, memory tests

Withdrawal intensifies craving

Yadid

Page 22: Epigenetic Mechanisms: Mediating Between Experience & Mental & Physical Health

DNA methylation changes following cocaine

administration, cues and withdrawal

Page 23: Epigenetic Mechanisms: Mediating Between Experience & Mental & Physical Health

Epigenetic modulation reprograms craving behavior only at

the end of a long withdrawal period when paired with a cue

Combined behavioral and epigenetic therapy

b

FIGURE 5

0

500

1000

1500

0

50

100

150

200

250

Training Test0

20

40

60

80

aCSF

RG108

Dis

tan

ce (cm

)

Tim

e in

op

en

arm

(sec)

caCSF

RG108

aCSF

RG108

Exp

lora

tio

n (%

)

d

0

20

40

60

80

** *

0

30

60

90

120 ****

a

Lever

pre

sses

D30 D60

D30 D60

aCSF

SAM

Lever

pre

sses

f

aCSF

RG108

0

30

60

90

120

e

Lever

pre

sses

Before injection

After injection

**

**

b

FIGURE 5

0

500

1000

1500

0

50

100

150

200

250

Training Test0

20

40

60

80

aCSF

RG108

Dis

tan

ce (cm

)

Tim

e in

op

en

arm

(sec)

caCSF

RG108

aCSF

RG108

Exp

lora

tio

n (%

)

d

0

20

40

60

80

** *

0

30

60

90

120 ****

a

Lever

pre

sses

D30 D60

D30 D60

aCSF

SAM

Lever

pre

sses

f

aCSF

RG108

0

30

60

90

120

e

Lever

pre

sses

Before injection

After injection

**

**

b

FIGURE 5

0

500

1000

1500

0

50

100

150

200

250

Training Test0

20

40

60

80

aCSF

RG108

Dis

tan

ce (cm

)

Tim

e in

op

en

arm

(sec)

caCSF

RG108

aCSF

RG108

Exp

lora

tio

n (%

)d

0

20

40

60

80

** *

0

30

60

90

120 ****

a

Lever

pre

sses

D30 D60

D30 D60

aCSF

SAM

Lever

pre

sses

f

aCSF

RG108

0

30

60

90

120

e

Lever

pre

sses

Before injection

After injection

**

**

RG108 DNA methyl transferase inhibitor

After long withdrawal immediately after training

SAM DNA methylation stimulator

Page 24: Epigenetic Mechanisms: Mediating Between Experience & Mental & Physical Health

ESR1 and CDK5 are modulated by DNA methylation inhibitors in the cocaine craving model; ESR1 agonist propyl pyrazole triol (PPT) and CDK5 antagonist (roscovitine) reverse cocaine craving

FIGURE 7

Cdk5chr4

0

-0.78

500 b

Esr1

27 kb

chr1

0

-0.39

Esr1

mRN

A

0.0

0.4

0.8

1.2 *aCSF roscovitine

CDK5 inhibitor

0

400

800

1200

0

30

60

90

120

150**

Leve

r pre

sses

Loco

mot

ion

0.0

0.4

0.8

1.2

1.6

aCSF PPT

ESR1 agonist

0

400

800

1200

0

20

40

60

80

100

Leve

r pre

sses

****

Loco

mot

ion

Cdk5

mRN

A

aCSF RG108

DNMT inhibitor

aCSF RG108

DNMT inhibitor

DNA

meth

ylatio

n DN

A m

ethyla

tion

a

b

FIGURE 7

Cdk5chr4

0

-0.78

500 b

Esr1

27 kb

chr1

0

-0.39

Esr1

mR

NA

0.0

0.4

0.8

1.2 *aCSF roscovitine

CDK5 inhibitor

0

400

800

1200

0

30

60

90

120

150**

Leve

r pre

sses

Loco

mot

ion

0.0

0.4

0.8

1.2

1.6

aCSF PPT

ESR1 agonist

0

400

800

1200

0

20

40

60

80

100

Leve

r pre

sses

****

Loco

mot

ion

Cdk

5 m

RN

A

aCSF RG108

DNMT inhibitor

aCSF RG108

DNMT inhibitor

DN

A m

ethy

latio

n D

NA

met

hyla

tion

a

b

Page 25: Epigenetic Mechanisms: Mediating Between Experience & Mental & Physical Health

What are the implications of a life-long dynamic

epigenome?

chemical social

Signaling pathways

phenotype

biosphere

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Page 26: Epigenetic Mechanisms: Mediating Between Experience & Mental & Physical Health

AcknowledgementsAnne McKiney

Tony Huang

Ziv Machnes

Gustavo Turecki

Michael Meaney

Ian Weaver

Patrick McGowan

Michael Hallett,

Matt Suderman

Stephen Suomi, Allyson Bennett, Peter Pierre

Nadine Provencal

Renaud Massart

Laura Stone

Lei Cao

Suzan King

Gal Yadid (BIU)

Renaud Massart

Royi Barnea (BIU)

Yahav Dikshtein (BIU)

Oren Meir (BIU)

Peter Gass

Michaela Schmidt

THIS RESEARCH IS SUPPORTED BYGRANTS FROM CIHR MRC, the Sackler program in

epigenetics and psychobiology